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Conservation 2009 (24): 91–97

Distribution of the Green Monkey ( sabaeus) in the Coastal Zone of Côte d’Ivoire

Sery Gonedelé Bi 1, 2, J. C. Koffi Bené 1, 3, E. Anderson Bitty 1,4, Inza Koné 1,4 and Dietmar Zinner5

¹Laboratoire de Génétique, Université d’Abidjan-Cocody, Côte d’Ivoire ²Centre Suisse de Recherches Scientifiques en Côte d’Ivoire ³Laboratoire de Zoologie, URES Université de Daloa, Côte d’Ivoire 4Laboratoire de Zoologie, Université d’Abidjan-Cocody, Côte d’Ivoire 5German Primate Center, Göttingen, Germany

Abstract: The green monkey (Chlorocebus sabaeus) of West ranges from the north-west coast of to the White Volta in Ghana. In Côte d’Ivoire, C. sabaeus was thought to be mainly distributed through the savannah and savannah-forest mosaic habitats north of the rain forest zone. During primate surveys in the forest zone of southern Côte d’Ivoire we were unable to confirm the presence ofC. sabaeus in any of the forest reserves; however, we did find the species in a littoral forest outside its expected range. Chlorocebus sabaeus was also reported from two other forests in the coastal region of Côte d’Ivoire. The discov- ery of these three populations is surprising and shows that there is an urgent need for more surveys in the region. The absence of C. sabaeus in areas where it was reported 30 years ago is another alarming indication concerning the conservation of in Côte d’Ivoire. Key words: Chlorocebus sabaeus, distribution, habitat, conservation status, Côte d’Ivoire

Résumé: L’aire de répartition du callitriche (Chlorocebus sabaeus) de l’Afrique de l’Ouest s’étend de la côte nord-ouest du Séné- gal à l’est jusqu’à l’Ouest du Volta blanc à l’ouest. En Côte d’Ivoire, son aire de distribution avait été confinée à la savane et aux mosaïques savane-forêts au Nord. Au cours de l’inventaire des primates dans la zone forestière au Sud de la Côte d’Ivoire, nous n’avons pu confirmer la présence de Chlorocebus spp. dans aucune des réserves forestières. Cependant, nous l’avons observé dans la forêt du littoral, en dehors de son aire de répartition connue. Aussi, la présence de Chlorocebus spp. a été rapportée dans deux autres forêts de la zone côtière de Côte d’Ivoire. La découverte de ces trois populations est surprenante et montre qu’il y a un besoin urgent de mener davantage d’inventaires dans la région. L’absence de Chlorocebus spp. dans des régions où il avait été rapporté plus de 30 ans auparavant est un autre signal alarmant concernant la conservation des primates de Côte d’Ivoire. Mots clés: Chlorocebus sabaeus; distribution; habitat; statut de conservation; Côte d’Ivoire

Introduction described (Hill 1966; Napier 1981; Kingdon 1997; Groves 2001). Their taxonomic status and phylogenetic relationships Savannah monkeys (Chlorocebus) are among the most remain unclear and the of the entire genus is in widespread of the African primates and inhabit large parts urgent need of a revision (Groves 2001). Even the generic of sub-Saharan Africa (Hill 1966; Wolfheim 1983; Lernould name is under discussion. Groves (2001) resurrected Chloro- 1988; Kingdon 1997). They are found across the continent cebus Gray, 1870, but Grubb et al. (2003) retained the genus from north-west Senegal to Eritrea, Djibouti and Somalia, as name Cercopithecus Linnaeus, 1758, regarding the former to well as southward over much of southern Africa. Chlorocebus be a synonym. In the present paper we follow Groves (2001) spp. live in a wide variety of habitats but show preference for and accept the generic name Chlorocebus. Among the various savannahs and savannah forest mosaics and are not found in taxa of the genus we find the Chlorocebus( aethiops), the moist forests of Central and , or in the deserts which occurs from south-eastern Sudan through Ethiopia into of south-west Africa (Hill 1966; Wolfheim 1983; Lernould Eritrea, the Bale Mountains monkeys (C. djamdjamensis) 1988; Kingdon 1997). Numerous morphotypes have been from a restricted area in the highlands of Ethiopia, the vervet

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(C. pygerythrus) from southern Ethiopia into the southern For Côte d’Ivoire, several authors have reported the part of Africa, the malbrouck (C. cynosuros) from southern distribution of C. sabaeus as being limited to the Guinean D. R. Congo, central Zambia and Angola, the tantalus monkey savannah north of the forest zone (Booth 1956, 1958; Hill (C. tantalus) in northern central Africa from the Volta River 1966; Galat and Galat-Luong 1980; Lernould 1988; King- in Ghana east into Sudan, Uganda and north-western Kenya, don 1997). Its presence in the Comoé National Park, north- and the green or callithrix monkey (C. sabaeus) in West eastern Côte d’Ivoire, for example, is well documented (Ger- Africa from Mauritania and Senegal to the western bank of ling and Bokdam 1973; Balzamo et al. 1980; Fischer et al. the Volta River in Ghana and Burkina Faso (Kingdon 1997; 1999-2000, 2002). The distribution of C. sabaeus in southern Groves 2001). Côte d’Ivoire, however, is not well known; only Tahiri-Zagrët The ecology and behaviour of savannah monkeys have (1976) had reported it to occur in parts of the southern forest been studied mainly in East and southern Africa (for example, zone. Here we report a population of C. sabaeus from the Struhsaker 1967; Henzi and Lucas 1980; Seyfarth et al. 1980; littoral forest of Iles Ehotilé National Park (NP), south Côte Wrangham and Waterman 1981; Cheney and Seyfarth 1983, d’Ivoire; a site outside the previously described range of this 1987; Isbell et al. 1991; Barrett et al. 2006), with consider- species. ably less information available for C. sabaeus and C. tanta- lus (for example, Dunbar 1974; Galat and Galat-Luong 1976, Methods 1977; Kavanagh 1978; Galat 1983; Harrison 1983; Nakagawa 2000, 2003). A number of studies of C. sabaeus have been Between 2000 and 2006 we conducted surveys in 23 conducted on Caribbean Islands, where introduced protected forests in southern Côte d’Ivoire (for a complete have established populations (Poirier 1972; Fairbanks 1978; list see Gonedelé Bi et al. submitted). All 23 forests have Horrocks 1986; Boulton et al. 1996). habitat suitable for primates (Gonedelé Bi 2008). The surveys

Figure 1. Distribution of savannah monkeys in West Africa, based on maps in Lernould (1988) and Kingdon (1997) (left, vertical hatching = C. sabaeus; right, horizontal hatching = C. tantalus; cross-hatching = possible overlap of both taxa). In Ghana, Côte d’Ivoire and Liberia, C. sabaeus is confined to the savannah habitats north of the rain forest region (but see Tahiri-Zagrët 1976).

92 Green monkey in Coastal Côte d’Ivoire

included extensive walks in the forests, along with interviews or acoustic signs of primates, determined the species present with hunters, officials and other local people from villages and recorded geographic positions with a global positioning surrounding the forests (for further details see Gonedelé Bi system. We were familiar with the appearance and behavior et al. 2006, 2008). We carried out foot surveys over 99 days of C. sabaeus from previous encounters with the species in in the 23 forests, with a mean of 4.13 survey days (range: 1 to Marahoué National Park (6°01'W, 7°07'N) and in Soko Forest 14 days) for each of the forests. In total, we covered 2,673 km. Grove (2°44'W, 7°58'N) (Fig. 1). We had also seen and exam- For each survey we formed three teams, each composed ined C. sabaeus carcasses in local markets. of a researcher and a local guide recruited among hunters, former hunters, or staff of the local bio-monitoring pro- Results grammes. The three teams surveyed different zones of the forests simultaneously so that a relatively large area was cov- During our survey in Iles Ehotilé National Park (550 ha) ered within a short period. Surveys normally lasted nine hours we sighted a group of five C. sabaeus on Elouamin Island (between 06:30 and 17:30) with a break from 12:00 to 14:00. (3°18'W, 5°09'N, c. 95 ha), one of the five islands compris- During surveys we walked slowly (1–1.25 km/hour) and qui- ing this reserve. We also found dead specimens of C. sabaeus etly along old logging roads and paths. We noted all visible among the bushmeat offered in a market in Assomlan, a

Figure 2. Geographical position of sites in Cote d’Ivoire where we encountered C. sabaeus (Marahoué National Park, Soko Forest Grove) or where it was reported outside its expected range, (Iles Ehotilé National Park, Port Gauthier Forest Reserve, and Bohico Forest Grove). Galat (1983) observed C. sabaeus near Jacqueville. Dashed line = approximate northern limit of evergreen forest zone (Peltre 1976).

93 Gonedelé Bi et al. village adjacent to the National Park (c. 0.7 km from the press). The current distribution of C. sabaeus in Côte d’Ivoire border). The presence of C. sabaeus in two other areas, the appears to be discontinuous: a northern savannah population Port Gauthier Forest Reserve (5°27'W, 5°08'N, c. 2,500 ha) and a coastal mangrove population with a distribution gap of and the Bohico Forest Grove (5°32'W, 5°08'N, c. 5 ha) was about 300 km in the interjacent forest zone. reported by several villagers. However, in the Port Gauth- The disjunct distribution of C. sabaeus in Côte d’Ivoire ier Forest Reserve we failed to find C. sabaeus during one is puzzling, and Galat and Galat-Luong (pers. comm.) sug- week of surveying. For the Bohico Forest Grove, we have gest that those living in and near the mangrove swamps of only information from interviews. All three sites are in the the coast descended from introduced pets. The lagoon forests forest zone of southern Côte d’Ivoire, outside the reported where C. sabaeus occurs are along the former north-south range of C. sabaeus (Fig. 2). We were unable to confirm the road to Abidjan and/or near important points of interest for presence of C. sabaeus in any of the forest reserves in south- tourists (exotic botanic garden and seaside resorts). These ern Côte d’Ivoire (see Gonedelé Bi et al. submitted) besides areas may have been used by foreigners to release pets before Soko Forest Grove and Marahoué National Park and the three leaving the country. Due to the considerable adaptability and reserves at the coast. the ability of C. sabaeus to colonize mangrove swamps, the released monkeys would be expected to survive and repro- Discussion duce in these areas (Galat and Galat-Luong 1976; Poirier 1972; McGuire 1974). Mangrove swamps in West Africa are The occurrence of C. sabaeus in the coastal forest zone becoming increasingly important refuges for large of Côte d’Ivoire is surprising since, according to a number as human populations increase (Galat-Luong and Galat 2007; of authors, it is confined to the savannah and savannah forest Gonedelé Bi et al. 2008). mosaics of the drier northern parts of the country, such as A second hypothesis sees the colonization of the coastal Comoé, Marahoué National Park and Sokala-Sobara, near area by C. sabaeus as a consequence of relatively recent Dabakala (Booth 1956, 1958; Hill 1966; Galat and Galat- human-caused conversion of the rain forest into a forest agri- Luong 1980; Lernould 1988; Kingdon 1997). Galat and culture mosaic. Savannah monkeys are known for invading Galat-Luong (in press) draw the southernmost bound- cultivated forests (Kavanagh 1980) and since large parts of ary of the geographical range of C. sabaeus at the south of the forests in southern Côte d’Ivoire are already converted, the “V Baoulé” savannah (for example, near Lakota, Divo there might now be a corridor for C. sabaeus to reach the and Tiassalé) and exclude forest areas such as Tai, Duékoué, coastal forests. If so, we would expect to also findC. sabaeus Soubré and the coastal forests. By contrast, Tahiri-Zagrët in areas between the northern savannah and the coastal region, (1976) reported C. sabaeus from Tai, Duékoué and Soubré. wherever the forest has been converted to cultivation. There Galat (1983), however, reported C. sabaeus from a site in the are, however, no reports of C. sabaeus from this region. coastal area; a group on the edge of the Ebrié Lagoon, near It might also be possible that the present populations of Jacqueville (c. 40 km west of Abidjan), whereas Tahiri-Zagrët C. sabaeus in the littoral forests are relicts from a former con- (1976) wrote that C. sabaeus does not occur in the coastal tinuous distribution of the species from the northern savannah areas of southern Côte d’Ivoire. A possible reason for this belt to the coastal areas. There is some evidence that climatic contradictory information may be that local people call both fluctuations during the Pleistocene caused several retreats and Lowe’s monkey Cercopithecus lowei and C. sabaeus “little expansions of rain forest in Côte d’Ivoire (Hewitt 2000). It black” or “little dark monkeys”, and often mistake one for is highly likely that savannah covered parts of southern Côte the other (Anh Galat-Luong and Gerard Galat, pers. comm.). d’Ivoire during this period, thus connecting the northern savan- Hence, it might be that the C. sabaeus reported from the forest nah with the coast (Maley 1996; Ray and Adams 2001; Leal area is indeed Cercopithecus lowei. 2004). Under such conditions, it would have been possible for During our surveys (Gonedelé Bi et al. 2006; Gonedelé C. sabaeus to disperse from northern savannahs south to coastal Bi 2008; Galat and Galat-Luong, in press; Gonedelé Bi et al. areas, where they subsisted in mangrove habitats after the re- in press) we did not encounter C. sabaeus in any protected grown rainforest isolated them from their northern conspecifics. area in the forest zone where the species was reported by A population genetic study, comparing northern and southern Tahiri-Zagrët (1976). This suggests that C. sabaeus has never C. sabaeus is underway to test hypotheses about the origin of occurred in these areas, has been locally extirpated, or that it the southern population and about the time of their isolation. is so rare that we did not find it. Our observations have con- Due to their wide distribution and large numbers, none firmed the presence of C. sabaeus near the coast, namely in of the five Chlorocebus spp. is regarded as threatened, with Ile Ehotilé National Park. the exception of C. djamdjamensis (see IUCN 2008). In Côte At this site (and also at the two other sites where d’Ivoire, however, even a generally common and adaptable C. sabaeus was reported by villagers) C. sabaeus seems to be species, such as C. sabaeus, has been apparently extirpated restricted to swamp forests and mangroves. The use of man- from large parts of its former range. This provides another groves by C. sabaeus has also been reported for populations example of the inadequate efforts to preserve primates in Côte in Senegal, Sierra Leone and Ghana (Galat and Galat-Luong d’Ivoire. The presence of C. sabaeus in the littoral forests 1976; Galat 1983; Grubb et al. 1998; Galat and Galat-Luong in of Côte d’Ivoire, on the other hand, demonstrates that more

94 Green monkey in Coastal Côte d’Ivoire

survey work has to be done to document primate diversity Galat, G. and A. Galat-Luong. 1976. La colonisation de la and distribution in this region of the country. The informa- mangrove par Cercopithecus aethiops sabaeus au Séné- tion obtained from such surveys needs to be considered in the gal. Rev. Ecol. Terre Vie 30: 3–30. development of conservation measures for the region. Galat, G. and A. Galat-Luong. 1977. Démographie et régime alimentaire d’une troupe de Cercopithecus aethiops Acknowledgements sabaeus en habitat marginal au Nord Sénégal. Rev. Ecol. Terre Vie 31: 557–577. We are grateful to the Ministère de l’Environnement et de Galat, G. and A. Galat-Luong. 1980. Données écologiques sur la Protection de la Nature of Côte d’Ivoire for permission to les Singes de la région de Dabakala et du Parc National conduct this study in Côte d’Ivoire’s national parks and forest de la Comoé, Côte d’Ivoire. Report, Office de la Recher- reserves. We also thank Bertin Akpatou and Zoro Goné Bi for che Scientifique et Technique d’Outre-Mer (ORSTOM), their help during the survey, and John F. Oates, Anh Galat- Adiopodoumé, Côte d’Ivoire. Luong, Gérard Galat, Jean-Marc Lernould, and Thomas M. Galat, G. 1983. Socio-écologie du singe vert (Cercopithecus Butynski for comments on earlier versions of the paper. This aethiops sabaeus), en référence de quatre Cercopithéci- work was supported in part by Centre Suisse de Recherches nés forestiers sympatriques (Cercocebus atys, Cercopi- Scientifiques (CSRS) and CEPA (Conservation des Espèces et thecus campbelli, C. diana, C. petaurista) d’Afrique de des Populations Animales). The study complied with l’Ouest. PhD thesis, Université Pierre et Marie Curie, care regulations and applicable national laws. Paris. Galat G. and A. Galat-Luong. In press. Green Monkey Chlo- Literature Cited rocebus sabaeus. In: The Mammals of Africa Vol. 2. Pri- mates, T. M. Butynski, J. Kingdon and J. Kalina (eds.). 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Authors’ addresses: Sery Gonedelé Bi, Laboratoire de Génétique, Université de Cocody Abidjan, Côte d’Ivoire, 22 BP 582 Abidjan 22 and Centre Suisse de Recherches Scientifiques en Côte d’Ivoire, 01 BP 1303 Abidjan 01, Côte d’Ivoire. E-mail: < gonedelebi@ yahoo.fr >. J. C. Koffi Bené, Laboratoire de Zoologie, URES Université de Daloa, BP 150 Daloa, Côte d’Ivoire, and Centre Suisse de Recherches Scientifiques en Côte d’Ivoire, 01 BP 1303 Abi- djan 01, Côte d’Ivoire. E-mail: < [email protected] >. E. Anderson Bitty, Laboratoire de Zoologie, Université de Cocody Abidjan, Côte d’Ivoire, 22 BP 582 Abidjan 22, and Centre Suisse de Recherches Scientifiques en Côte d’Ivoire, 01 BP 1303 Abidjan 01, Côte d’Ivoire. E-mail: < anderson. [email protected] >. Inza Koné, Laboratoire de Zoologie, Université de Cocody Abidjan, Côte d’Ivoire, 22 BP 582 Abidjan 22 and Centre Suisse de Recherches Scientifiques en Côte d’Ivoire, 01 BP 1303 Abidjan 01, Côte d’Ivoire. E-mail: < inza.kone@csrs. ci >. Dietmar Zinner, Deutsches Primatenzentrum, Kellnerweg 4, 37077 Göttingen, Germany. E-mail: < [email protected] >. (Corresponding author).

Received for publication: 25 May 2009 Revised: 9 September 2009

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